Diversification of MIF immune regulators in aphids: link with agonistic and antagonistic interactions

Abstract

BackgroundThe widespread use of genome sequencing provided evidences for the high degree of conservation in innate immunity signalling pathways across animal phyla. However, the functioning and evolutionary history of immune-related genes remains unknown for most invertebrate species. A striking observation coming from the analysis of the pea aphid Acyrthosiphon pisum genome is the absence of important conserved genes known to be involved in the antimicrobial responses of other insects. This reduction in antibacterial immune defences is thought to be related to their long-term association with beneficial symbiotic bacteria and to facilitate symbiont maintenance. An additional possibility to avoid elimination of mutualistic symbionts is a fine-tuning of the host immune response. To explore this hypothesis we investigated the existence and potential involvement of immune regulators in aphid agonistic and antagonistic interactions.ResultsIn contrast to the limited antibacterial arsenal, we showed that the pea aphid Acyrthosiphon pisum expresses 5 members of Macrophage Migration Inhibitory Factors (ApMIF), known to be key regulators of the innate immune response. In silico searches for MIF members in insect genomes followed by phylogenetic reconstruction suggest that evolution of MIF genes in hemipteran species has been shaped both by differential losses and serial duplications, raising the question of the functional importance of these genes in aphid immune responses. Expression analyses of ApMIFs revealed reduced expression levels in the presence, or during the establishment of secondary symbionts. By contrast, ApMIFs expression levels significantly increased upon challenge with a parasitoid or a Gram-negative bacteria. This increased expression in the presence of a pathogen/parasitoid was reduced or missing, in the presence of facultative symbiotic bacteria.ConclusionsThis work provides evidence that while aphid’s antibacterial arsenal is reduced, other immune genes widely absent from insect genomes are present, diversified and differentially regulated during antagonistic or agonistic interactions.Electronic supplementary materialThe online version of this article (doi:10.1186/1471-2164-15-762) contains supplementary material, which is available to authorized users.

A Secreted MIF Cytokine Enables Aphid Feeding and Represses Plant Immune Responses

“…Sequence similarities among aphid MIFs are more pronounced between identical members from different species (orthologs) than between different members of the same species (paralogs; Figure S1). This is consistent with previous results showing a complex evolutionary history, which is characterized by differential gene loss and duplication across insect phyla and which occurred before the diversification of aphids [10].…”

“…Here, we show the existence and expression of three MIF members in the green peach aphid Myzus percicae, which we named MpMIF1 (GenBank: KP218519), MpMIF3 (GenBank: KR136352), and MpMIF4 (GenBank: KR136353) according to their sequence similarities with the A. pisum MIFs [10]. Sequence similarities among aphid MIFs are more pronounced between identical members from different species (orthologs) than between different members of the same species (paralogs; Figure S1).…”

“…Aphids Secrete a MIF1 Salivary Protein We previously showed [10] that the pea aphid Acyrthosiphon pisum expresses five members of a MIF multigene family (ApMIF1-ApMIF5; Figure 1A). Here, we show the existence and expression of three MIF members in the green peach aphid Myzus percicae, which we named MpMIF1 (GenBank: KP218519), MpMIF3 (GenBank: KR136352), and MpMIF4 (GenBank: KR136353) according to their sequence similarities with the A. pisum MIFs [10].…”

Plant Immune Responses: Aphids Strike Back

“…Naessens and colleagues [11], in their new study, focus on the role of MIFs from the pea aphid, Acyrthosiphon pisum, and from the green peach aphid, Myzus persicae. In a previous study, the same group searched the recently available A. pisum genome for immune regulators and discovered the presence of five genes coding for MIFs [13]. ApMIFs were expressed in circulating immune cells and are upregulated after pathogen and parasitoid infection, implying a role in host immune response [13].…”

“…In a previous study, the same group searched the recently available A. pisum genome for immune regulators and discovered the presence of five genes coding for MIFs [13]. ApMIFs were expressed in circulating immune cells and are upregulated after pathogen and parasitoid infection, implying a role in host immune response [13]. Here, Naessens et al [11] observe that one member of the ApMIF family, ApMIF1, and its homologue MpMIF1 from M. persicae are expressed in salivary glands and that the corresponding MIF proteins are secreted during feeding.…”